Abstract
The heat shock protein 70 (Hsp70) family members are known as molecular chaperones. They play a crucial role in protecting plant cells and tissues from thermal or abiotic stress through protein folding and in assembly, stabilization, activation, and degradation processes. Although many studies have been performed to identify molecular functions of individual family members, there is a limited study on genome-wide identification and characterizations of Hsps in the Populus model tree genus. We have identified 34 poplar Hsp70 genes, which were phylogenetically clustered into three major groups. Gene structure and motif composition are relatively conserved in each group. Mainly tandem and infrequently segmental duplications have a significant role in poplar Hsp70 gene expansion. The in silico microRNA (miRNA) and target transcript analyses identified that a total of 19 PtHsp70 genes were targeted by 27 plant miRNAs. PtHSP70-14 and PtHSP70-33 are the most targeted by miR390 and miR414 family members, respectively. For determination of drought response to Hsp70 genes, publicly available RNA-seq data were analyzed. Poplar Hsp70s are differentially expressed upon exposure to different drought stress conditions. Expression analysis of PtHsp70 genes was also examined under drought stress in drought-sensitive and drought-resistant Populus clones with quantitative real-time PCR (qRT-PCR). PtHsp70-16 and PtHsp70-26 genes might provide adaptation to drought stress for both clones. Because of high expression responses to drought in only resistant Populus clone, PtHsp70-25 and PtHsp70-33 genes might be used for determination of drought-tolerant clones for molecular breeding studies. This research provides a fundamental clue for contribution of PtHsp70s to drought tolerance in poplar.
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References
Alvim FC, Carolino SM, Cascardo JC, Nunes CC, Martinez CA, Otoni WC, Fontes EP (2001) Enhanced accumulation of BiP in transgenic plants confers tolerance to water stress. Plant Physiol 126:1042–1054
Axtell MJ, Jan C, Rajagopalan R, Bartel DP (2006) A two-hit trigger for siRNA biogenesis in plants. Cell 127:565–577
Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34:W369–373
Baloglu MC, Inal B, Kavas M, Unver T (2014a) Diverse expression pattern of wheat transcription factors against abiotic stresses in wheat species. Gene 550(1):117–122
Baloglu MC, Eldem V, Hajyzadeh M, Unver T (2014b) Genome-Wide analysis of the bZIP transcription factors in Cucumber. PLoS One 9(4):e96014. doi:10.1371/journal.pone.0096014
Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE (2000) The protein data bank. Nucleic Acids Res 28:235–242
Boston RS et al (1996) Molecular chaperones and protein folding in plants. Plant Mol Biol 32:191–222. doi:10.1007/BF00039383
Budak H, Akpinar BA, Unver T, Turktas M (2013) Proteome changes in wild and modern wheat leaves upon drought stress by two-dimensional electrophoresis and nanoLC-ESI–MS/MS. Plant Mol Biol 1–15
Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10
Caraux G, Pinloche S (2005) PermutMatrix: a graphical environment to arrange gene expression profiles in optimal linear order. Bioinformatics Applications Note 21(7):1280–1281. doi:10.1093/bioinformatics/bti141
Caruso A, Chefdor F, Carpin S, Depierreux C, Delmotte FM, Kahlem G, Morabito D (2008) Physiological characterization and identification of genes differentially expressed in response to drought induced by PEG 6000 in Populus canadensis leaves. J Plant Physiol 165:932–941. doi:10.1016/j.jplph.2007.04.006
Cho EK, Choi YJ (2009) A nuclear-localized HSP70 confers thermoprotective activity and drought-stress tolerance on plants. Biotechnol Lett 31:597–606
Cohen D, Bogeat-Triboulot MB, Tisserant E, Balzergue S, Martin-Magniette ML, Lelandais G, Ningre N, Renou JP, Tamby JP, Le Thiec D et al (2010) Comparative transcriptomics of drought responses in Populus: a metaanalysis of genome-wide expression profiling in mature leaves and root apices across two genotypes. BMC Genomics 11(1):630
Conesa A, Götz S (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 619832. doi: 10.1155/2008/619832
Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674–3676
Cossu RM, Giordani T, Cavallini A, Natali L (2014) High-throughput analysis of transcriptome variation during water deficit in a poplar hybrid: a general overview. Tree Genetics & Genomes 10:53–66. doi:10.1007/s11295-013-0661-5
Dhankher OP, Drew JE, Gatehouse JA (1997) Characterisation of a pea Hsp70 gene which is both developmentally and stress-regulated. Plant Mol Biol 34(2):345–52
Du D, Zhang Q, Cheng T, Pan H, Yang W et al (2013) Genome-wide identification and analysis of late embryogenesis abundant (LEA) genes in Prunus mume. Mol Biol Rep 40(2):1937–46. doi:10.1007/s11033-012-2250-3
Eulgem T et al (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206
Chen F, Hayes PM, Mulrooney DM, Pan A (1994) Nucleotide sequence of a cDNA encoding a heat-shock protein (HSP70) from barley (Hordeum vulgare L.). Plant Physiol 106(2):815
Feist AM, Palsson BO (2008) The growing scope of applications of genome-scale metabolic reconstructions using Escherichia coli. Nat Biotechnol 26:659–667. doi:10.1038/nbt1401
Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD et al (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186. doi:10.1093/nar/gkr944
Guleria P, Yadav SK (2011) Identification of miR414 and expression analysis of conserved miRNAs from Stevia rebaudiana. Genomics Proteomics Bioinformatics 9(6):211–217. doi:10.1016/S1672-0229(11)60024-7
Guo AY, Zhu QH, Chen X, Luo JC (2007) GSDS: a gene structure display server. Yi Chuan 29:1023–1026. doi:10.1360/yc-007-1023
Gurley WB (2000) HSP101: a key component for the acquisition of thermotolerance in plants. Plant Cell 12:457–460
Hartl FU (1996) Molecular chaperones in cellular protein folding. Nature 381:571–580. doi:10.1038/381571a0
Hendrick JP, Hartl F (1993) Molecular chaperone functions of heat-shock proteins. Annu Rev Biochem 62:349–384. doi:10.1146/annurev.bi.62.070193.002025
Hill JE, Hemmingsen SM (2001) Arabidopsis thaliana type I and II chaperonins. Cell Stress Chaperon 6(3):190–200
Hu W, Hu G, Han B (2009) Genome-wide survey and expression profiling of heat shock proteins and heat shock factors revealed overlapped and stress specific response under abiotic stresses in rice. Plant Sci 176(4):583–590
Jain M, Nijhawan A, Arora R, Agarwal P, Ray S et al (2007) F-Box Proteins in Rice. genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. Plant Physiol 143:14671483. doi:10.1104/pp. 106.091900
Jakoby M, Weisshaar B, Droge-Laser W, Vicente-Carbajosa J, Tiedemann J et al (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7(3):106–111. doi:10.1016/s1360-1385(01)02223-3
Jansson S, Douglas CJ (2007) Populus: a model system for plant biology. Annu Rev Plant Biol 58:435–458. doi:10.1146/annurev.arplant.58.032806.103956
Jefferys BR, Kelley LA, Sternberg MJE (2010) Protein folding requires crowd control in a simulated cell. J Mol Biol 397:1329–1338. doi:10.1016/j.jmb.2010.01.074
Jung KH, Gho HJ, Nguyen MX, Kim SR, An G (2013) Genome-wide expression analysis of HSP70 family genes in rice and identification of a cytosolic HSP70 gene highly induced under heat stress. Funct Integr Genomics 13(3):391–402. doi:10.1007/s10142-013-0331-6
Jungkunz I, Link K, Vogel F, Voll LM, Sonnewald S, Sonnewald U (2011) AtHsp70-15-deficient Arabidopsis plants are characterized by reduced growth, a constitutive cytosolic protein response and enhanced resistance to TuMV. Plant J 66:983–995
Kampinga HH, Craig EA (2010) The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol 11:579–592. doi:10.1038/nrm2941
Kavas M, Baloğlu MC, Atabay ES, Tanman Ziplar U, Yıldız Daşgan H, Ünver T (2015) Genome-wide characterization and expression analysis of common bean bHLH transcription factors in response to excess salt concentration. Mol Genet Genomics. doi:10.1007/s00438-015-1095-6
Kelley LA, Sternberg MJE (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4:363–371
Kotak S, Larkindale J, Lee U, von Koskull-Döring P, Vierling E, Scharf KD (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310–316. doi:10.1016/j.pbi.2007.04.011
Krishna P, Gloor G (2001) The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperone 6(3):238–246
Kumar R, Nagarajan NS, Arunraj SP et al (2012) HSPIR: a manually annotated heat shock protein information resource. Bioinformatics Applications Note 28(21):2853–2855. doi:10.1093/bioinformatics/bts520
Lecharny A, Boudet N, Gy I, Aubourg S, Kreis M (2003) Introns in, introns out in plant gene families: a genomic approach of the dynamic of gene structure. J Struct Funct Genomics 3:111–116
Lee U, Rioflorido I, Hong SW, Larkindale J, Waters ER, Vierling E (2007) The Arabidopsis ClpB/Hsp100 family of proteins: chaperones for stress and chloroplast development. Plant J 49(1):115–127
Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res. doi:10.1093/nar/gkr931
Lin BL, Wang JS, Liu HC, Chen RW, Meyer Y, Barakat A, Delseny M (2001) Genomic analysis of the Hsp70 superfamily in Arabidopsis thaliana. Cell Stress Chaperones 6(3):201–208
Livak JK, Schmittgen TD (2001) Analysis of relative gene expression data using realtime quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408
Lund PA (2001) Molecular chaperones in the cell. Oxford University Press, Oxford
Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155. doi:10.1126/science.290.5494.1151
Marron N, Delay D, Petit JM, Dreyer E, Kahlem G, Delmotte FM, Brignolas F (2002) Physiological traits of two Populus×euramericana clones, Luisa Avanzo and Dorskamp, during a water stress and re-watering cycle. Tree Physiol 22:849–858. doi:10.1093/treephys/22.12.849
Maruyama D, Endo T, Nishikawa S (2010) BiP-mediated polar nuclei fusion is essential for the regulation of endosperm nuclei proliferation in Arabidopsis thaliana. Proc Natl Acad Sci USA 107:1684–1689
Mehan MR, Freimer NB, Ophoff RA (2004) A genome-wide survey of segmental duplications that mediate common human genetic variation of chromosomal architecture. Hum Genomics 1(5):335–344
Monclus R, Dreyer E, Villar M, Delmotte FM, Delay D, Petit JM, Barbaroux C, Thiec D, Brechet C, Brignolas F (2006) Impact of drought on productivity and water use efficiency in 29 genotypes of Populus deltoides×Populus nigra. New Phytol 169:765–777. doi:10.1111/j.1469-8137.2005.01630.x
Neill SJ, Burnett EC (1999) Regulation of gene expression during water deficit stress. Plant Growth Regul 29:23–33. doi:10.1023/a:1006251631570
Nijhawan A, Jain M, Tyagi AK, Khurana JP (2008) Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol 146:333–350. doi:10.1104/pp. 107.112821
Noel LD, Cagna G, Stuttmann J, Wirthmuller L, Betsuyaku S, Witte CP, Bhat R, Pochon N, Colby T, Parker JE (2007) Interaction between SGT1 and cytosolic/nuclear HSC70 chaperones regulates Arabidopsis immune responses. Plant Cell 19:4061–4076
Park CJ, Bart R, Chern M, Canlas PE, Bai W, Ronald PC (2010) Overexpression of the endoplasmic reticulum chaperone BiP3 regulates XA21-mediated innate immunity in rice. PLoS One 5:e9262. doi:10.1371/journal.pone.0009262
Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant Sci 17:1360–1385. doi:10.1016/j.tplants.2012.02.004
Qi Y, Wang H, Zou Y, Liu C, Liu Y, Wang Y, Zhang W (2011) Overexpression of mitochondrial heat shock protein 70 suppresses programmed cell death in rice. FEBS Lett 585:231–239
Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N et al (2005) InterProScan: protein domains identifier. Nucleic Acids Res 33:W116–W120. doi:10.1093/nar/gki442
Rochester DE, Winer JA, Shah DM (1986) The structure and expression of maize genes encoding the major heat-shock protein, Hsp70. EMBO J 5:451–458
Romanel EA et al (2009) Evolution of the B3 DNA binding superfamily: new insights into REM family gene diversification. PLoS One 4:e5791
Rouard M, Guignon V, Aluome C, Laporte MA, Droc G, Walde C, Zmasek CM, Perin C, Conte MG (2011) GreenPhylDB v2.0: comparative and functional genomics in plants. Nucleic Acids Res 39:D1095–D1102
Sarkar NK, Kundnani P, Grover A (2013) Functional analysis of Hsp70 superfamily proteins of rice (Oryza sativa). Cell Stress Chaperones 18(4):427–437
Scharf KD, Siddique M, Vierling E (2001) The expanding family of Arabidopsis thaliana small heat stress proteins and a new family of proteins containing alpha-crystallin domains (Acd proteins). Cell Stress Chaperones 6(3):225–237
Schlesinger MJ (1990) Heat shock proteins. J Biol Chem 265(21):12111–12114
Schöffl F, Prandl R, Reindl A (1998) Regulation of the heat shock response. Plant Physiol 117:1135–1141. doi:10.1104/pp.117.4.1135
Shiu SH, Bleecker AB (2003) Expansion of the receptor-like kinase/pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132:530–543. doi:10.1104/pp. 103.021964
Söding J (2005) Protein homology detection by HMM-HMM comparison. Bioinformatics 21:951–960. doi:10.1093/bioinformatics/bti125
Song H, Zhao R, Fan P, Wang X, Chen X, Li Y (2009) Overexpression of AtHsp90.2, AtHsp90.5 and AtHsp90.7 in Arabidopsis thaliana enhances plant sensitivity to salt and drought stresses. Planta 229(4):955–964
Song YP, Wang ZL, Bo WH, Ren YY, Zhang ZY, Zhang DQ (2012) Transcriptional profiling by cDNA-AFLP analysis showed differential transcript abundance in response to water stress in Populus hopeiensis. BMC Genomics 13:286. doi:10.1186/1471-2164-13-286
Su PH, Li HM (2008) Arabidopsis stromal 70-kD heat shock proteins are essential for plant development and important for thermotolerance of germinating seeds. Plant Physiol 146:1231–1241
Sung DY, Vierling E, Guy CL (2001) Comprehensive expression profile analysis of the Arabidopsis Hsp70 gene family. Plant Physiol 126(2):789–800
Suo J et al (2003) Identification of GhMYB109 encoding a R2R3MYB transcription factor that expressed specifically in fiber initials and elongating fibers of cotton (Gossypium hirsutum L.). Biochim Biophys Acta 1630:25–34
Suyama M, Torrents D, Bork P (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34:W609–W612. doi:10.1093/nar/gkl315
Tamura K, Peterson D, Peterson N, Stecher G, Nei M et al (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121
Tang H, Bowers JE, Wang X, Ming R, Alam M et al (2008) Synteny and collinearity in plant genomes. Science 320:486–488. doi:10.1126/science.1153917
Tang S, Dong Y, Liang D et al (2014) Analysis of the drought stress-responsive transcriptome of Black Cottonwood (Populus trichocarpa) using deep rna sequencing. Plant Mol Biol Rep. doi:10.1007/s11105-014-0759-4
Tang S, Liang H, Donghui Y et al (2013) Populus euphratica: the transcriptomic response to drought stress. Plant Mol Biol 83:539–557. doi:10.1007/s11103-013-0107-3
Thompson JD, Gibson TJ, Plewniak F et al (1997) The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. doi:10.1093/nar/25.24.4876
Török Z, Goloubinoff P, Horwáth I et al (2001) Synechocystis HSP17 is an amphitropic protein that stabilizes heat-stressed membranes and binds denatured proteins for subsequent chaperone-mediated refolding. Proc Natl Acad Sci USA 98:3098–3103. doi:10.1073/pnas.051619498
Turktas M, Inal B, Okay S, Erkilic EG et al (2013) Nutrition metabolism plays an important role in the alternate bearing of the olive tree (Olea europaea L.). PLoS ONE 8(3):e59876. doi:10.1371/journal.pone.0059876
Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313(5793):1596–1604. doi:10.1126/science.1128691
Vierling E (1991) The role of heat shock proteins in plants. Annu Rev Plant Phys 42:579–620. doi:10.1146/annurev.pp. 42.060191.003051
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78. doi:10.1093/jhered/93.1.77
Wakasa Y, Yasuda H, Oono Y, Kawakatsu T, Hirose S, Takahashi H, Hayashi S, Yang L, Takaiwa F (2011) Expression of ER quality control-related genes in response to changes in BiP1 levels in developing rice endosperm. Plant J 65:675–689
Wang Y, Lin S, Song Q, Li K, Tao H et al (2014) Genome-wide identification of heat shock proteins (Hsps) and Hsp interactors in rice: Hsp70s as a case study. BMC Genomics 15:344. doi:10.1186/1471-2164-15-344
Wang J, Zhou J, Zhang B, Vanitha J, Ramachandran S et al (2011) Genome-wide expansion and expression divergence of the basic leucine zipper transcription factors in higher plants with an emphasis on sorghum. J Integr Plant Biol 53(3):212–231. doi:10.1111/j.1744-7909.2010.01017.x
Wang X, Liu W, Chen X, Tang C et al (2010) Differential gene expression in incompatible interaction between wheat and stripe rust fungus revealed by cDNA -AFLP and comparison to compatible interaction. BMC Plant Biol 10:9. doi:10.1186/1471-2229-10-9
Waters ER, Lee GJ, Vierling E (1996) Evolution, structure and function of the small heat shock proteins in plants. J Exp Bot 47:325–338. doi:10.1093/jxb/47.3.325
Yang Z, Gu S, Wang X, Li W, Tang Z et al (2008) Molecular evolution of the cpp-like gene family in plants: insights from comparative genomics of Arabidopsis and rice. J Mol Evol 67:266–277. doi:10.1007/s00239-008-9143-z
Yildirim K (2013) Transcriptional and physiological responses to drought stress in Populus nigra L. Dissertation, Middle East Technical University
Zhang Y (2005) miRU: an automated plant miRNA target prediction server. Nucleic Acids Res 33 (Web Server issue) W701–4
Zhang J, Li J, Liu B, Zhang L, Chen J, Lu M (2013) Genome-wide analysis of the Populus Hsp90 gene family reveals differential expression patterns, localization, and heat stress responses. BMC Genomics 14:532. doi:10.1186/1471-2164-14-532
Zhang Y, Wang M, Chen J, Rong J, Ding M (2014) Genome-wide analysis of HSP70 superfamily in Gossypium raimondii and the expression of orthologs in Gossypium hirsutum. Yi Chuan 36(9):921–33. doi:10.3724/SP.J.1005.2014.0921. (Article in Chinese)
Zhang J, Liu B, Li J, Zhang L, Wang Y, Zheng H, Lu M, Chen J (2015) Hsf and Hsp gene families in Populus: genome-wide identification, organization and correlated expression during development and in stress responses. BMC Genomics 16:181. doi:10.1186/s12864-015-1398-3
Acknowledgments
This work was financially supported by the Kastamonu University Scientific Research Project Management Coordination Unit under Grant No: KÜBAP-01/2014-09. We would like to thank Dr. Tuncay PORSUK from Director of Inner Anatolia Forestry Research Institute for his help in providing the Populus nigra L. clones.
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ESM 1
Fig. S1 Examples of P. nigra drought resistant and sensitive clones used in the experiments. SC = Sensitive clone-control, ST = Sensitive clone-drought treated, RC = Resistant clone-control, RT = Resistant clone-drought treated. Asterisks indicate leaves (healthy, fully expanded, at approximately 6–10 nodes from the apex) collected for RNA isolation. (JPEG 377 kb)
ESM 2
Fig. S2 Percentage of Hsp70 genes on each poplar chromosome to show their distribution abundance. (JPEG 36 kb)
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Fig. S3 Schematic representation of conserved motifs (obtained using MEME) in Hsp70 proteins. Different motifs are represented as differently-colored boxes at the N-terminal and C-terminal region for the transcription regulatory region. (JPEG 197 kb)
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Fig. S4 Exon/intron structures of the PtHsp70 genes. The Hsp70 family members were classified according to Fig. 2. The values in parentheses show the number of corresponding classes of Hsp70 genes. Green boxes represent exons and black lines represent introns. (JPEG 274 kb)
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Fig. S5 Comparative physical mapping of Hsp70 genes in different organisms. Comparative physical mapping revealed high degree of orthologous relationships of Hsp70 genes located on chromosomes of poplar with (A) Arabidopsis, (B) rice, (C) maize and (D) grapevine. (JPEG 223 kb)
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Table S1. Summary of Hsp70 gene family factors of plants (XLSX 11 kb)
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Table S2. The Ka/Ks ratios and estimated divergence-time for tandemly-duplicated Hsp70 proteins. (DOCX 18 kb)
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Table S3. The Ka/Ks ratios and estimated divergence time for segmentally-duplicated Hsp70 proteins. (DOCX 29 kb)
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Table S4. Amino acid composition of the poplar Hsp70 motifs. Single letters of the motif match that letter; and the letter groups in square brackets match any letters in the group. (DOCX 15 kb)
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Table S5. Blast2Go annotation details of Hsp70 protein sequences. (XLSX 15 kb)
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Table S6. The Ka/Ks ratios and estimated divergence time for orthologous Hsp70 proteins between poplar, Arabidopsis, rice, maize and grapevine. (DOCX 16 kb)
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Table S7. miRNA targets identified by psRNA Target. (XLSX 16 kb)
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Table S8. Reliability and the residue percentage of 28 candidate HSP 70 proteins chosen for homology modeling. (DOC 36 kb)
ESM 14
Table S9. List of primers used in quantitative real-time-PCR expression analysis of Hsp70 genes. (DOC 35 kb)
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Yer, E.N., Baloglu, M.C., Ziplar, U.T. et al. Drought-Responsive Hsp70 Gene Analysis in Populus at Genome-Wide Level. Plant Mol Biol Rep 34, 483–500 (2016). https://doi.org/10.1007/s11105-015-0933-3
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DOI: https://doi.org/10.1007/s11105-015-0933-3